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BREAST IMAGING REPORTING AND DATA SYSTEM – BI-RADS®:

POSITIVE PREDICTIVE VALUE OF CATEGORIES 3, 4 AND 5.

A SYSTEMATIC LITERATURE REVIEW*

Fabíola Procaci Kestelman1

, Gustavo Antônio de Souza2

, Luiz Claudio Thuler3

, Gabriela Martins4 , Vivianne Aguilera Rolim de Freitas4

, Ellyete de Oliveira Canella5

OBJECTIVE: To review the literature about the positive predictive value of Breast Imaging Reporting and Data System (BI-RADS®) categories 3, 4 and 5. MATERIALS AND METHODS: A research was performed in the online Medline database, entering the terms “predictive value” and “BI-RADS”. Eleven studies were in-cluded in this review. RESULTS: The positive predictive values ranged respectively between 0% and 8%, 4% and 62%, and 54% and 100% for BI-RADS® categories 3, 4 and 5. Three studies have also evaluated morphological criteria with higher positive predictive value in mammography, mass with spiculated margins being the finding with highest positive predictive value for malignancy. CONCLUSION: A high variability was found in the reviewed literature among positive predictive values of BI-RADS® categories 3, 4 and 5, al-though methodological differences have been identified, limiting the comparative analysis.

Keywords: Mammography; BI-RADS®; Breast cancer.

Breast Imaging Reporting and Data System – BI-RADS®: valor preditivo positivo das categorias 3, 4 e 5. Revisão sistemática da literatura.

OBJETIVO: Avaliar artigos, na literatura, que verificam o valor preditivo positivo das categorias 3, 4 e 5 do Breast Imaging Reporting and Data System (BI-RADS®). MATERIAIS E MÉTODOS: Foi realizada pesquisa na base de dados Medline utilizando os termos “predictive value” e “BI-RADS”. Foram incluídos 11 artigos nesta revisão. RESULTADOS: O valor preditivo positivo das categorias 3, 4 e 5 variou entre 0% e 8%, 4% e 62%, 54% e 100%, respectivamente. Três artigos avaliaram, concomitantemente, os critérios morfológicos das lesões que apresentaram maior valor preditivo positivo na mamografia, sendo nódulo espiculado o critério com maior valor preditivo positivo. CONCLUSÃO: Houve grande variabilidade do valor preditivo positivo das categorias 3, 4 e 5 do BI-RADS® em todos os estudos, porém foram identificadas diferenças metodológicas que limitaram a comparação desses estudos.

Unitermos: Mamografia; BI-RADS®; Câncer de mama.

Abstract

Resumo

* Study developed at Service of Radiology, Hospital do Cân-cer III, Instituto Nacional de CânCân-cer-Ministério da Saúde (INCA-MS), Rio de Janeiro, RJ, Brazil.

1. MD, Radiologist at Hospital do Câncer III, Instituto Nacio-nal de Câncer-Ministério da Saúde (INCA-MS) and Clínica Radio-lógica Luiz Felippe Mattoso, Rio de Janeiro, RJ, Brazil.

2. Titular Professor at Department of Tocogynecology, Facul-dade de Ciências Médicas – UniversiFacul-dade Estadual de Campi-nas (FCM-Unicamp), CampiCampi-nas, SP, Brazil.

3. MD, Epidemiologist at Instituto Nacional de Câncer-Minis-tério da Saúde (INCA-MS), Associate Professor at Universidade Federal do Estado do Rio de Janeiro (Unirio), Rio de Janeiro, RJ, Brazil.

4. MDs, Radiologists at Hospital do Câncer III, Instituto Nacio-nal de Câncer-Ministério da Saúde (INCA-MS), Rio de Janeiro, RJ, Brazil.

5. Head of the Service of Radiology, Hospital do Câncer III, Instituto Nacional de Câncer-Ministério da Saúde (INCA-MS), Rio de Janeiro, RJ, Brazil.

Mailing address: Dra. Fabíola Procaci Kestelman. Rua Bogari, 82, ap. 201, Lagoa. Rio de Janeiro, RJ, Brazil, 22471-340. E-mail: fabkest@hotmail.com

Received July 11, 2005. Accepted after revision November 20, 2005.

cident type of cancer, according to Instituto Nacional de Câncer statistics(1). The

de-crease in mortality rate depends on an early detection, an adequate therapeutic plan-ning, and the adoption of the annual mam-mography as screening method(2).

Mammography presents high sensitiv-ity in the detection of clinically occult breast cancer. A review of clinical trials evaluating the performance of the method has demonstrated that the sensitivity ranged between 71% and 98% for the annual screening mammography(3). However,

many lesions deemed suspicious with in-dication for histopathological evaluation correspond to benign alterations. In the United States, the positive predictive value (PPV) of biopsies performed because of mammographic findings, that is to say, the total of diagnosed malignant lesions in re-lation to the total number of biopsies per-formed, ranges between 15% and 40%(4–6).

The cost and morbidity of the procedures for the diagnosis of these lesions are taken into consideration to confirm the adoption of mammography as a screening method(7).

One of the difficulties in the evaluation of mammograms is that the greatest part of the diagnosed lesions does not present pathognomonic characteristics. Knutzen & Gisvold(8) have studied the probability of

malignancy in several categories of non-palpable lesions detected by mammogra-phy, and observed that, if the morphologi-cal criteria of these lesions were taken into consideration, the rate of malignant lesions among women submitted to biopsy could reach 40%.

Aiming at reducing the discordance in the interpretation of mammographic find-ings and standardizing the terms for char-acterization and reporting, the American College of Radiology published, in 1993, the Breast Imaging Reporting and Data

INTRODUCTION

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in-System (BI-RADS®)(9). New editions were

released in 1995, 1998 and 2003(10–12).

According to the latest (fourth) edition of BI-RADS®(12), the studies are classified

with basis on the lesions’ suspicion level into: category 1 – without positive find-ings; category 2 – benign findfind-ings; egory 3 – probably benign findings; cat-egory 4 – suspicious findings; catcat-egory 5 – findings highly suggestive of malignancy. Lesions requiring additional evaluation, for example with ultrasound, are classified into category 0, and those with previously con-firmed histopathological diagnosis of ma-lignancy, into category 6.

The BI-RADS® latest edition included

suggestions for evaluation of breast lesions with ultrasound and magnetic resonance imaging. Notwithstanding its great utility already observed in relation to the BI-RADS® for mammography, the use of this lexicon is still recent, generating some criti-cism and considerations(13,14).

Some studies evaluate the capacity to predict malignancy of categories 3, 4 and 5 where lesions presenting some level of suspicion would be included. A way to evaluate the performance of each BI-RADS® category is to analyse the results

of lesions submitted to biopsy, and calcu-late the PPV considering the histopatho-logical result as the gold-standard.

This literature review is aimed at evalu-ating the PPV of BI-RADS® categories 3,

4 and 5. Additionally, morphological crite-ria utilized for stratification of lesions were analyzed.

MATERIALS AND METHODS

The literature review was performed by means of a search in the online Medline database, by entering the terms “predictive value” and “BI-RADS®”. The publications

included in the present review have met the following criteria: original articles evalu-ating the PPV of BI-RADS® categories 3,

4 and 5; PPV analysis based on histopatho-logical results; studies published from 1998; papers written in Portuguese, En-glish or French. Studies evaluating only one or two categories, or whose online ab-stract was not available were excluded.

The selected original articles were inte-grally evaluated in order to confirm their

compliance with the above mentioned cri-teria. Nine of the 33 studies found in the search have met these criteria. By means of the bibliographic references in these nine studies, we have found other two compli-ant studies, totalling 11 articles.

The data extracted from the articles were registered on an Excel® (Microsoft)

worksheet. The following items were in-cluded: study period; number of lesions evaluated; patients’ages; type of lesion (palpable/non-palpable); biopsy method; clinical, radiological or surgical manage-ment of the lesions submitted to percuta-neous biopsy; PPV of BI-RADS® catego-ries 3, 4 and 5; morphological criteria analysis.

The categories’ PPVs have been ex-tracted from the articles or calculated through the data available, considering the number of lesions in one of the categories with malignant diagnosis divided by the total number of lesions classified into this category, and finally multiplied by 100. In this case, the histological results classified as malignant were ductal carcinoma in situ or any other primary, invasive breast tumor, according to BI-RADS® recommenda-tions(12).

Only one study has evaluated both le-sions submitted to some biopsy method and lesions under radiological follow-up. In this case, the PPV was calculated consid-ering only the lesions initially submitted to biopsy(15), with the histopathological

crite-ria as the gold-standard.

RESULTS

The 11 articles reviewed reported the data required for determination of catego-ries 3, 4 and 5 PPV. Data from these stud-ies are summarized in Table 1.

In three articles, information was ob-tained exclusively from patients submitted to surgical biopsy(16–18). Five studies

re-ported the assessment of patients submit-ted to percutaneous biopsy(19–23), and two

studies evaluated results of patients submit-ted to percutaneous biopsy and patients submitted to surgical biopsy in conjunc-tion(15,24). Liberman et al. have studied

separately patients submitted to percutane-ous biopsy and patients submitted to sur-gical biopsies(25).

Ta b le 1 S tu d ie s o n b re a st le si o n s w ith P P V f o r B I-R A D S

® ca

te g o ri e s 3 , 4 a n d 5 . St u d y Li b e rm a n e t a l. (2 5 ), 1 9 9 8 B é ru b é e t a l. (1 9 ), 1 9 9 8 O re l e t a l. (1 6 ), 1 9 9 9 La cq u e m e n t e t a l. (2 4 ), 1 9 9 9 Ta te e t a l. (2 0 ), 2 0 0 1 M a rg o lin e t a l. (2 1 ), 2 0 0 1 B a ll e t a l. (1 7 ), 2 0 0 2 Tr a va d e e t a l. (2 2 ), 2 0 0 2 M e n d e z e t a l. (2 3 ), 2 0 0 3 Ta n e t a l. (1 8 ), 2 0 0 4 Z o n d e rl a n d e t a l. (1 5 ), 2 0 0 4 P e ri o d Ja n ./ 1 9 9 6 – No v. /1 9 9 6 Ju l. /1 9 9 4 – Ju n ./ 1 9 9 5 A p r. /1 9 9 1 – D e c ./ 1 9 9 6 Ja n ./ 1 9 9 5 – Ju n ./ 1 9 9 7 F e b ./ 1 9 9 4 – D e c ./ 1 9 9 9 Ja n ./ 1 9 9 4 – D e c ./ 1 9 9 8 Ja n ./ 1 9 9 4 – Ju n ./ 1 9 9 9 O c t. /1 9 9 9 – Ja n ./ 2 0 0 1 A u g ./ 2 0 0 0 – D e c ./ 2 0 0 2 Ja n ./ 1 9 9 5 – D e c ./ 2 0 0 0 Ju n ./ 2 0 0 0 – Ju n ./ 2 0 0 1

N 49

2 1 9 3 4 9 5 1 ,3 1

2 68

1 ,0 8 0 1 ,3 3 3 1 0 9 2 5 2 9 4 7 4 9 7 2 1 0 A g e (y e a rs ) 2 7 – 9 2

? 22

8

9

? ? 31

8

8

? 37

– 9 0 2 9 – 8 0 2 5 – 8 9 3 1 – 8 5 2 1 – 9 2 P h ys ic a l e xa m in a ti o n No n -p a lp a b le

? ? No

n -p a lp a b le P a lp a b le a n d n o n -p a lp a b le

? Pa

lp a b le a n d n o n -p a lp a b le No n -p a lp a b le No n -p a lp a b le

? Pa

lp a b le a n d n o n -p a lp a b le P a lp a b le a n d n o n -p a lp a b le B io p sy m e th o d

SB PB

( CB a n d M T) P B ( CB ) SB SB a n d P B ( F NA B , CB a n d M T) P B ( CB , M T a n d A B B I) P B ( CB a n d M T)

SB PB

( M T) P B ( M T) SB SB a n d P B ( F NA B , CB ) Ca rc in o m a s p re va le n c e 4 6 % 3 7 % 1 2 % 3 4 % 2 3 % 1 8 % 1 1 % 3 8 % 2 8 % 1 6 % 1 6 % 5 4 % P P V a cc o rd in g t o B I-RA D S

® c

a te g o ry B I-RA D S

® 3

0 % (0 /8 ) 0 % (0 /2 ) 0 % (0 /1 6 ) 2 % (3 /1 4 1 ) 3 % (9 /3 2 2 ) 2 % (2 /8 7 ) 3 % (1 /3 4 ) 0 % (0 /1 0 ) 0 % (0 /1 2 ) 4 % (7 /1 5 6 ) 5 % (1 0 /2 0 1 ) 8 % (4 /4 9 ) B I-RA D S

® 4

3 4 % (1 2 0 /3 5 5 ) 1 8 % (2 5 /1 4 1 ) 4 % (1 7 /3 9 7 ) 3 0 % (2 7 9 /4 3 6 ) 2 3 % (5 4 /2 3 4 ) 1 7 % (1 5 9 /9 6 1 ) 1 0 % (1 0 0 /9 6 7 ) 2 6 % (1 8 /6 8 ) 2 0 % (4 1 /2 0 6 ) 1 5 % (1 1 6 /7 5 7 ) 2 7 % (4 9 /1 8 0 ) 6 2 % (3 9 /6 2 ) B I-RA D S

® 5

(3)

As regards the studies based on percu-taneous biopsies, four of them refer to the follow-up of patients both by radiological follow-up of lesions with benign cal diagnosis, and by analysis of histologi-cal results from later surgihistologi-cal biopsies, for example, in cases with initial histological diagnosis of atypical ductal hyperpla-sia(20-22,25). In the other studies, these data are incomplete. Bérubé et al.(19) have

re-ported a new biopsy in cases where there was disagreement between the histological report and the radiological aspect of the lesion. Two studies have correlated histo-logical results of atypical hyperplasia with those of surgical biopsy(23,24). Zonderland

et al.(15) describe the clinical management

of lesions by means of data from de insti-tution itself and from a national register of histopathological studies results.

As regards selection of patients consid-ering the physical examination of their breasts, the studies have not followed a homogeneous criterion. Eight of them re-port physical examination, with four evalu-ating only non-palpable lesions(16,17,22,25)

and the others have report assessment of both palpable and non-palpable le-sions(15,18,21,24). Three articles have not

clearly described the type of lesions stud-ied(19,20,23), however, they have assessed

patients submitted to ultrasound- or stereo-tactic-guided percutaneous biopsy, which may indicate that these lesion are clinically occult. In the study where Liberman et al.(25) have evaluated patients submitted to

percutaneous biopsy, these data are not sufficiently defined, but the lesions have also been submitted to ultrasound- or ster-eotactic-guided biopsy.

PPV of categories 3, 4 and 5

In the 11 studies, the PPV ranged be-tween 0% and 8% for category 3 (median, 2%), 4% and 63% for category 4 (median, 21%), and between 54% and 100% for category 5 (median, 89%)(Figure 1). In the four studies where the method for obtain-ing the histopathological result was exclu-sively surgical biopsy, the PPV found for categories 3, 4 and 5 ranged, respectively, between 0% and 5%, 26% and 34%, and between 81% and 97%(16–18,25). In the six

studies evaluating lesions submitted only to percutaneous biopsy, the PPV for

cat-egories 3, 4 and 5 ranged, respectively, tween 0% and 4%, 4% and 20%, and be-tween 54% and 92%(19–23,25).

The four studies evaluating only non-palpable lesions(16,17,22,25) presented a PPV

variation, for category 3, between 0% and 2%, for category 4, between 20% and 34%, and, for category 5, between 77% and 97%. The four articles reporting results from palpable and non-palpable lesions(15,18,21,24) demonstrated a PPV variation, for category 3, between 3% and 8%, for category 4, between 10% and 63%, and for category 5, between 84% and 100%.

Morphological criteria with higher PPV

Three articles have mentioned the mor-phological characteristics of the lesions with major association with malignancy. Liberman et al.(25) and Bérubé et al.(19) have

evaluated morphological characteristics of lesions as proposed by the second edition of BI-RADS®(12), including, for analysis of

masses, the evaluation of margins and shape, and for calcifications, the morphol-ogy and distribution (Table 2). Mendez et

al.(23) have classified the lesions into microcalcifications, asymmetrical density, circumscribed mass, spiculated or with microcalcifications, and asymmetrical den-sity with microcalcifications. In the three studies, spiculated mass has been the lesion with highest PPV(19,23,25). As regards masses, Liberman et al.(25) have observed

that the criteria with higher PPV were spiculated margins and irregular shape; and, as regards microcalcifications, were linear morphology and segmental or linear distribution. Bérubé et al.(19) have reported

that the morphological criteria with higher PPV were dense masses, massed with spi-culated margins, and linear microcalcifi-cations.

DISCUSSION

The studies analyzed with the purpose of evaluating the PPV for BI-RADS®

cat-egories 3, 4 and 5 demonstrated a signifi-cant difference in the cancer detection among these categories. However, the methodology utilized in those studies was

Table 2 Radiological findings with highest PPV, according to BI-RADS®.

Study

Liberman et al.(25), 1998

Bérubé et al.(19), 1998

Morphological criteria

Mass with spiculated margin Irregularly shaped mass

Microcalcifications with linear morphology Microcacifications with segmental distribution Microcalcifications with linear distribution

Dense mass

Mass with spiculated margin

Microcalcifications with linear morphology

PPV

81% 73% 81% 74% 68%

90% 91% 80% Figure 1. Positive predictive values reported in studies for BI-RADS® categories.

BI-RADS

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quite heterogeneous, limiting the compari-son between results. Some studies pre-sented limited information regarding pa-tients selection. Some of them do not men-tion if the lesions were palpable or non-palpable. In the articles where there is no reference to the type of the studied lesions, the histopathological result was obtained by means of ultrasound- or stereotactic-guided percutaneous biopsy, suggesting that the lesions were clinically occult. The variation of the carcinomas prevalence in these studies and, consequently, of PPV for categories, may be related with the differ-ences in the selection of patients for surgi-cal or percutaneous biopsy.

Another factor that may influence the carcinomas prevalence is the radiological follow-up of lesions with benign histo-pathological diagnosis. In studies with fol-low-up of patients after core needle (14 gauge) biopsy, the frequency of non-diag-nosed carcinomas ranged between 0.3% and 8.2%, and, with the radiological fol-low-up, 70% of these carcinomas were immediate false negative, and 30%, de-layed false negative(26,27).

Additionally, as regards the number of carcinomas diagnosed by percutaneous biopsy, another variable should be consid-ered: the management of underestimated lesions. For example, a lesion diagnosed as atypical ductal hyperplasia, after percuta-neous biopsy, may correspond to a ductal carcinoma in situ or an invasive ductal car-cinoma. As regards lesions diagnosed as atypical ductal hyperplasia, when submit-ted to core needle (14 gauge) biopsy, 20% to 56% correspond to carcinomas in surgi-cal biopsies, while 0% to 38% of lesions submitted to directional vacuum-assisted biopsy (mammotomy) with 14- or 11-gauge needle are underestimated as atypi-cal ductal hyperplasia. These data demon-strate that, when the volume of biopsy tis-sue acquired is higher, the underestimation rate is lower, although not non-existent(28).

Considering these data, the studies ana-lyzed also demonstrate heterogeneous char-acteristics. Six(15,20,22–25) of the eight

ar-ticles(15,19–25) where the histopathological

results have been obtained from lesions submitted to percutaneous biopsy report the radiological follow-up of benign le-sions and surgical biopsy of determined

benign lesions, for example, atypical duc-tal hyperplasia. Considering that these two variables affect the number of malignant diagnoses, studies presenting homogeneity between these aspects may show differ-ences in their results.

Another important factor for the analy-sis of the categories´ PPV is related to the use of BI-RADS®, which may be limited by deficiencies in the classification or training of radiologists(29,30). Berg et al.(31) have

evaluated inter- and intraobserver variabil-ity in the utilization of the BI-RADS®

ter-minology. Five mammography-experi-enced radiologists have assessed 103 rou-tine mammograms. The rate of agreement among the radiologists (kappa statistical method) ranged between 0.16 and 0.77 for the several mammographic findings, show-ing moderate variability, and 0.37 for BI-RADS® categories, corresponding to poor agreement. Orel et al.(16), analyzing the

mammographic findings in different insti-tutions, have observed that some patients referred for biopsy presented benign le-sions classified as BI-RADS® category 2

and, therefore, biopsy would not be indi-cated. This discrepancy was associated with the interobserver variation, both for describing the lesions and for recommend-ing biopsy, and also was associated with variations in the experience of the radiolo-gists involved in the mammograms analy-sis. Bérubé et al.(19) have associated the low

PPV obtained for category 4 with the fact of the BI-RADS® nomenclature being

de-scriptive and poorly specific.

Contrarily to Bérubé et al.(19),

Zonder-land et al.(15) have found higher PPVs for

all the categories, in comparison with re-sults found in American studies. This find-ing has been attributed to the fact that, in the American studies, there is a tendency to get a higher number of positive diag-noses based on biopsy in order to reduce the number of false-negative results from mammography. This affects the selection of patients for histopathological investigation. The same finding is reported by a study comparing routine mammograms per-formed in the United States and in the United Kingdom(32).

As regards PPVs of categories, the BI-RADS®suggests values below 2% for

cat-egory 3 and above 95% for catcat-egory 5,

while five studies have found values above the one suggested for category 3(15,18,21, 23,24)

, and in nine articles the values were lower than expected for category 5(17–25).

Finally, the present review demonstrates that in all of the studies there was a high variability in PPVs of BI-RADS®

catego-ries 3, 4 and 5. The comparison among re-sults from the 11 studies is limited by the heterogeneity in the criteria for patients selection, biopsy methods, and, in the case of the studies with results from percutane-ous biopsy, by the heterogeneity in the ra-diological follow-up of both benign and underestimated lesions. However, there is a scale for malignancy prediction allowing the definition, with a relative assurance, of patients with higher risk of breast cancer. Additionally, the studies demonstrate that the presence of spicutated mass presents a high association with malignancy.

Acknowledgments

Our thanks to the physicians at the sec-tor of breast imaginology of Clínica Luiz Felippe Mattoso, Erika Esteves Araújo Torres, MD, Márcia Costa Jazbik, MD, Karla Dias de Paiva, MD, and Marcela Leite Balaro, MD, for their contribution to the present study; to Doctor Professor Sophie Derchain, MD, researcher at Centro de Atenção Integral à Saúde da Mulher – Universidade Estadual de Campinas (Caism-Unicamp), for supervising the present study.

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17. Ball CG, Butchart M, MacFarlane JK. Effect on biopsy technique of the breast imaging reporting and data system (BI-RADS) for nonpalpable mammographic abnormalities. Can J Surg 2002; 45:259–263.

18. Tan YY, Wee SB, Tan MP, Chong BK. Positive predictive value of BI-RADS categorization in an Asian population. Asian J Surg 2004;27:186–191. 19. Bérubé M, Curpen B, Ugolini P, Lalonde L, Oui-met-Oliva D. Level of suspicion of a mammo-graphic lesion: use of features defined by BI-RADS lexicon and correlation with large-core breast biopsy. Can Assoc Radiol J 1998;49:223-–228.

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28. Liberman L. Percutaneous image-guided core breast biopsy. Radiol Clin North Am 2002;40: 483–500.

29. Liberman L, Menell JH. Breast Imaging Report-ing and Data System (BI-RADS). Radiol Clin North Am 2002;40:409–430.

30. Godinho ER, Koch HA. Breast Imaging Report-ing and Data System (BI-RADS™): como tem sido utilizado? Radiol Bras 2004;37:413–417. 31. Berg WA, Campassi C, Langenberg P, Sexton MJ.

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Imagem

Table 2 Radiological findings with highest PPV, according to BI-RADS ® . Study

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Considerando o modelo de jogo como a tradução teórico-prática da forma de “jogar” idealizada pelo treinador em função das características do clube e dos seus jogadores, Garganta

17,18 Regarding the treatment of intralabyrinthine schwannomas, in most of the cases reported in the selected studies, clini- cal and serial radiological follow-up was

This scenario, coupled with the existence of protocols and recommendations for diagnosis and follow-up of hypertension patients elaborat- ed by the Ministry of Health,